The X and Y Chromosomes Assemble into H2A.Z, Containing Facultative Heterochromatin, following Meiosis

REFERENCES

• Abbott, D. W., M. Laszczak, J. D. Lewis, H. Su, S. C. Moore, M. Hills, S. Dimitrov, and J. Ausio. 2004. Structural characterization of macroH2A containing chromatin. Biochemistry 43:1352–1359.
   PubMed Web of Science ®Google Scholar
• Armstrong, S. J., M. A. Hulten, A. M. Keohane, and B. M. Turner. 1997. Different strategies of X-inactivation in germinal and somatic cells: histone H4 underacetylation does not mark the inactive X chromosome in the mouse male germline. Exp. Cell Res. 230:399–402.
   PubMedGoogle Scholar
• Bruce, K., F. A. Myers, E. Mantouvalou, P. Lefevre, I. Greaves, C. Bonifer, D. J. Tremethick, A. W. Thorne, and C. Crane-Robinson. 2005. The replacement histone H2A.Z in a hyperacetylated form is a feature of active genes in the chicken. Nucleic Acids Res. 33:5633–5639.
   PubMed Web of Science ®Google Scholar
• Bulynko, Y., L. C. Hsing, R. W. Mason, D. J. Tremethick, and S. A. Grigoryev. 2006. Cathepsin L stabilizes histone modification landscape on Y chromosome and pericentric heterochromatin. Mol. Cell. Biol. 26:4172–4184.
   PubMedGoogle Scholar
• Byrne, J. A., S. Simonsson, P. S. Western, and J. B. Gurdon. 2003. Nuclei of adult mammalian somatic cells are directly reprogrammed to oct-4 stem cell gene expression by amphibian oocytes. Curr. Biol. 13:1206–1213.
   PubMed Web of Science ®Google Scholar
• Champion, M. D., and R. S. Hawley. 2002. Playing for half the deck: the molecular biology of meiosis. Nat. Med. 8(Suppl.):S50–S56.
   Google Scholar
• Churikov, D., J. Siino, M. Svetlova, K. Zhang, A. Gineitis, E. Morton Bradbury, and A. Zalensky. 2004. Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics 84:745–756.
   PubMedGoogle Scholar
• Churikov, D., I. A. Zalenskaya, and A. O. Zalensky. 2004. Male germline-specific histones in mouse and man. Cytogenet. Genome Res. 105:203–214.
   PubMed Web of Science ®Google Scholar
• Costanzi, C., and J. R. Pehrson. 1998. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393:599–601.
   PubMed Web of Science ®Google Scholar
• Costanzi, C., P. Stein, D. M. Worrad, R. M. Schultz, and J. R. Pehrson. 2000. Histone macroH2A1 is concentrated in the inactive X chromosome of female preimplantation mouse embryos. Development 127:2283–2289.
   PubMed Web of Science ®Google Scholar
• Cowell, I. G., R. Aucott, S. K. Mahadevaiah, P. S. Burgoyne, N. Huskisson, S. Bongiorni, G. Prantera, L. Fanti, S. Pimpinelli, R. Wu, D. M. Gilbert, W. Shi, R. Fundele, H. Morrison, P. Jeppesen, and P. B. Singh. 2002. Heterochromatin, HP1, and methylation at lysine 9 of histone H3 in animals. Chromosoma 111:22–36.
   PubMed Web of Science ®Google Scholar
• Echeverri, K., and E. M. Tanaka. 2002. Mechanisms of muscle dedifferentiation during regeneration. Semin. Cell Dev. Biol. 13:353–360.
   PubMed Web of Science ®Google Scholar
• Faast, R., V. Thonglairoam, T. C. Schulz, J. Beall, J. R. Wells, H. Taylor, K. Matthaei, P. D. Rathjen, D. J. Tremethick, and I. Lyons. 2001. Histone variant H2A.Z is required for early mammalian development. Curr. Biol. 11:1183–1187.
   PubMed Web of Science ®Google Scholar
• Fan, J. Y., F. Gordon, K. Luger, J. C. Hansen, and D. J. Tremethick. 2002. The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states. Nat. Struct. Biol. 9:172–176.
   PubMedGoogle Scholar
• Fan, J. Y., D. Rangasamy, K. Luger, and D. J. Tremethick. 2004. H2A.Z alters the nucleosome surface to promote HP1α-mediated chromatin fiber folding. Mol. Cell 16:655–661.
   PubMed Web of Science ®Google Scholar
• Fernandez-Capetillo, O., S. K. Mahadevaiah, A. Celeste, P. J. Romanienko, R. D. Camerini-Otero, W. M. Bonner, K. Manova, P. Burgoyne, and A. Nussenzweig. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4:497–508.
   PubMed Web of Science ®Google Scholar
• Francastel, C., D. Schubeler, D. I. Martin, and M. Groudine. 2000. Nuclear compartmentalization and gene activity. Nat. Rev. Mol. Cell. Biol. 1:137–143.
   PubMedGoogle Scholar
• Gatewood, J. M., G. R. Cook, R. Balhorn, C. W. Schmid, and E. M. Bradbury. 1990. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J. Biol. Chem. 265:20662–20666.
   PubMed Web of Science ®Google Scholar
• Govin, J., C. Caron, C. Lestrat, S. Rousseaux, and S. Khochbin. 2004. The role of histones in chromatin remodeling during mammalian spermiogenesis. Eur. J. Biochem. 271:3459–3469.
   PubMedGoogle Scholar
• Greaves, I. K., M. Svartman, M. Wakefield, D. Taggart, A. De Leo, M. A. Ferguson-Smith, W. Rens, P. C. O'Brien, L. Voullaire, M. Westerman, and J. A. Graves. 2001. Chromosomal painting detects non-random chromosome arrangement in dasyurid marsupial sperm. Chromosome Res. 9:251–259.
   PubMed Web of Science ®Google Scholar
• Grigoryev, S. A., T. Nikitina, J. R. Pehrson, P. B. Singh, and C. L. Woodcock. 2004. Dynamic relocation of epigenetic chromatin markers reveals an active role of constitutive heterochromatin in the transition from proliferation to quiescence. J. Cell Sci. 117:6153–6162.
   PubMed Web of Science ®Google Scholar
• Guillemette, B., A. R. Bataille, N. Gevry, M. Adam, M. Blanchette, F. Robert, and L. Gaudreau. 2005. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 3:e384.
   PubMed Web of Science ®Google Scholar
• Gurdon, J. B., J. A. Byrne, and S. Simonsson. 2003. Nuclear reprogramming and stem cell creation. Proc. Natl. Acad. Sci. USA 100(Suppl. 1):11819–11822.
   PubMed Web of Science ®Google Scholar
• Hazzouri, M., C. Pivot-Pajot, A. K. Faure, Y. Usson, R. Pelletier, B. Sele, S. Khochbin, and S. Rousseaux. 2000. Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur. J. Cell Biol. 79:950–960.
   PubMed Web of Science ®Google Scholar
• Hendriksen, P. J., J. W. Hoogerbrugge, A. P. Themmen, M. H. Koken, J. H. Hoeijmakers, B. A. Oostra, T. van der Lende, and J. A. Grootegoed. 1995. Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev. Biol. 170:730–733.
   PubMedGoogle Scholar
• Hoyer-Fender, S., C. Costanzi, and J. R. Pehrson. 2000. Histone macroH2A1.2 is concentrated in the XY-body by the early pachytene stage of spermatogenesis. Exp. Cell Res. 258:254–260.
   PubMedGoogle Scholar
• Hoyer-Fender, S., E. Czirr, R. Radde, J. M. Turner, S. K. Mahadevaiah, J. R. Pehrson, and P. S. Burgoyne. 2004. Localisation of histone macroH2A1.2 to the XY-body is not a response to the presence of asynapsed chromosome axes. J. Cell Sci. 117:189–198.
   PubMed Web of Science ®Google Scholar
• Khalil, A. M., F. Z. Boyar, and D. J. Driscoll. 2004. Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis. Proc. Natl. Acad. Sci. USA 101:16583–16587.
   PubMedGoogle Scholar
• Khil, P. P., N. A. Smirnova, P. J. Romanienko, and R. D. Camerini-Otero. 2004. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat. Genet. 36:642–646.
   PubMedGoogle Scholar
• Kierszenbaum, A. L., and L. L. Tres. 1974. Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J. Cell Biol. 63:923–935.
   PubMed Web of Science ®Google Scholar
• Kobor, M. S., S. Venkatasubrahmanyam, M. D. Meneghini, J. W. Gin, J. L. Jennings, A. J. Link, H. D. Madhani, and J. Rine. 2004. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2:e131.
   PubMed Web of Science ®Google Scholar
• Krogan, N. J., M. C. Keogh, N. Datta, C. Sawa, O. W. Ryan, H. Ding, R. A. Haw, J. Pootoolal, A. Tong, V. Canadien, D. P. Richards, X. Wu, A. Emili, T. R. Hughes, S. Buratowski, and J. F. Greenblatt. 2003. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 12:1565–1576.
   PubMed Web of Science ®Google Scholar
• Lachner, M., R. J. O'Sullivan, and T. Jenuwein. 2003. An epigenetic road map for histone lysine methylation. J. Cell Sci. 116:2117–2124.
   PubMed Web of Science ®Google Scholar
• Lewis, J. D., D. W. Abbott, and J. Ausio. 2003. A haploid affair: core histone transitions during spermatogenesis. Biochem. Cell Biol. 81:131–140.
   PubMed Web of Science ®Google Scholar
• Li, B., S. G. Pattenden, D. Lee, J. Gutierrez, J. Chen, C. Seidel, J. Gerton, and J. L. Workman. 2005. Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc. Natl. Acad. Sci. USA 102:18385–18390.
   PubMedGoogle Scholar
• Loriot, A., T. Boon, and C. De Smet. 2003. Five new human cancer-germline genes identified among 12 genes expressed in spermatogonia. Int. J. Cancer 105:371–376.
   PubMedGoogle Scholar
• Ma, Y., S. B. Jacobs, L. Jackson-Grusby, M. A. Mastrangelo, J. A. Torres-Betancourt, R. Jaenisch, and T. P. Rasmussen. 2005. DNA CpG hypomethylation induces heterochromatin reorganization involving the histone variant macroH2A. J. Cell Sci. 118:1607–1616.
   PubMedGoogle Scholar
• Martens, J. H., R. J. O'Sullivan, U. Braunschweig, S. Opravil, M. Radolf, P. Steinlein, and T. Jenuwein. 2005. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24:800–812.
   PubMed Web of Science ®Google Scholar
• McCarrey, J. R., C. Watson, J. Atencio, G. C. Ostermeier, Y. Marahrens, R. Jaenisch, and S. A. Krawetz. 2002. X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse. Genesis 34:257–266.
   PubMedGoogle Scholar
• Metzler-Guillemain, C., J. Luciani, D. Depetris, M. R. Guichaoua, and M. G. Mattei. 2003. HP1β and HP1γ, but not HP1α, decorate the entire XY body during human male meiosis. Chromosome Res. 11:73–81.
   PubMedGoogle Scholar
• Meyer-Ficca, M., J. Muller-Navia, and H. Scherthan. 1998. Clustering of pericentromeres initiates in step 9 of spermiogenesis of the rat (Rattus norvegicus) and contributes to a well defined genome architecture in the sperm nucleus. J. Cell Sci. 111:1363–1370.
   PubMedGoogle Scholar
• Mizuguchi, G., X. Shen, J. Landry, W. H. Wu, S. Sen, and C. Wu. 2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343–348.
   PubMed Web of Science ®Google Scholar
• Motzkus, D., P. B. Singh, and S. Hoyer-Fender. 1999. M31, a murine homolog of Drosophila HP1, is concentrated in the XY body during spermatogenesis. Cytogenet. Cell Genet. 86:83–88.
   PubMedGoogle Scholar
• Oakberg, E. F. 1956. A description of spermiogenesis in the mouse and its use in analysis of the cell cycle of the seminiferous epithelium and germ cell renewal. Am. J. Anat. 99:391–413.
   PubMedGoogle Scholar
• Oliva, R., and G. H. Dixon. 1991. Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog. Nucleic Acids Res. Mol. Biol. 40:25–94.
   PubMed Web of Science ®Google Scholar
• Peters, A. H., S. Kubicek, K. Mechtler, R. J. O'Sullivan, A. A. Derijck, L. Perez-Burgos, A. Kohlmaier, S. Opravil, M. Tachibana, Y. Shinkai, J. H. Martens, and T. Jenuwein. 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12:1577–1589.
   PubMed Web of Science ®Google Scholar
• Peters, A. H., D. O'Carroll, H. Scherthan, K. Mechtler, S. Sauer, C. Schofer, K. Weipoltshammer, M. Pagani, M. Lachner, A. Kohlmaier, S. Opravil, M. Doyle, M. Sibilia, and T. Jenuwein. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337.
   PubMed Web of Science ®Google Scholar
• Peters, A. H., A. W. Plug, M. J. van Vugt, and P. de Boer. 1997. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5:66–68.
   PubMedGoogle Scholar
• Raisner, R. M., P. D. Hartley, M. D. Meneghini, M. Z. Bao, C. L. Liu, S. L. Schreiber, O. J. Rando, and H. D. Madhani. 2005. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123:233–248.
   PubMed Web of Science ®Google Scholar
• Rangasamy, D., L. Berven, P. Ridgway, and D. J. Tremethick. 2003. Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. EMBO J. 22:1599–1607.
   PubMedGoogle Scholar
• Rangasamy, D., I. Greaves, and D. J. Tremethick. 2004. RNA interference demonstrates a novel role for H2A.Z in chromosome segregation. Nat. Struct. Mol. Biol. 11:650–655.
   PubMed Web of Science ®Google Scholar
• Reinke, V. 2004. Sex and the genome. Nat. Genet. 36:548–549.
   PubMedGoogle Scholar
• Rice, J. C., S. D. Briggs, B. Ueberheide, C. M. Barber, J. Shabanowitz, D. F. Hunt, Y. Shinkai, and C. D. Allis. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12:1591–1598.
   PubMed Web of Science ®Google Scholar
• Richler, C., S. K. Dhara, and J. Wahrman. 2000. Histone macroH2A1.2 is concentrated in the XY compartment of mammalian male meiotic nuclei. Cytogenet. Cell Genet. 89:118–120.
   PubMedGoogle Scholar
• Ridgway, P., K. D. Brown, D. Rangasamy, U. Svensson, and D. J. Tremethick. 2004. Unique residues on the H2A.Z containing nucleosome surface are important for Xenopus laevis development. J. Biol. Chem. 279:43815–43820.
   PubMedGoogle Scholar
• Singer-Sam, J., M. O. Robinson, A. R. Bellve, M. I. Simon, and A. D. Riggs. 1990. Measurement by quantitative PCR of changes in HPRT, PGK-1, PGK-2, APRT, MTase, and Zfy gene transcripts during mouse spermatogenesis. Nucleic Acids Res. 18:1255–1259.
   PubMed Web of Science ®Google Scholar
• Solari, A. J. 1976. The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes. Chromosoma 29:217–236.
   Google Scholar
• Stargell, L. A., J. Bowen, C. A. Dadd, P. C. Dedon, M. Davis, R. G. Cook, C. D. Allis, and M. A. Gorovsky. 1993. Temporal and spatial association of histone H2A variant hv1 with transcriptionally competent chromatin during nuclear development in Tetrahymena thermophila. Genes Dev. 7:2641–2651.
   PubMedGoogle Scholar
• Turner, B. M., A. J. Birley, and J. Lavender. 1992. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69:375–384.
   PubMed Web of Science ®Google Scholar
• Turner, J. M., O. Aprelikova, X. Xu, R. Wang, S. Kim, G. V. Chandramouli, J. C. Barrett, P. S. Burgoyne, and C. X. Deng. 2004. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr. Biol. 14:2135–2142.
   PubMed Web of Science ®Google Scholar
• Turner, J. M., P. S. Burgoyne, and P. B. Singh. 2001. M31 and macroH2A1.2 colocalize at the pseudoautosomal region during mouse meiosis. J. Cell Sci. 114:3367–3375.
   PubMedGoogle Scholar
• Turner, J. M., S. K. Mahadevaiah, D. J. Elliott, H. J. Garchon, J. R. Pehrson, R. Jaenisch, and P. S. Burgoyne. 2002. Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist. J. Cell Sci. 115:4097–4105.
   PubMed Web of Science ®Google Scholar
• Turner, J. M., S. K. Mahadevaiah, O. Fernandez-Capetillo, A. Nussenzweig, X. Xu, C. X. Deng, and P. S. Burgoyne. 2005. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 37:41–47.
   PubMed Web of Science ®Google Scholar
• Ueno, M., T. Murase, T. Kibe, N. Ohashi, K. Tomita, Y. Murakami, M. Uritani, T. Ushimaru, and M. Harata. 2004. Fission yeast Arp6 is required for telomere silencing, but functions independently of Swi6. Nucleic Acids Res. 32:736–741.
   PubMedGoogle Scholar
• Wang, P. J., J. R. McCarrey, F. Yang, and D. C. Page. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27:422–426.
   PubMed Web of Science ®Google Scholar
• Zalensky, A. O., J. W. Breneman, I. A. Zalenskaya, B. R. Brinkley, and E. M. Bradbury. 1993. Organization of centromeres in the decondensed nuclei of mature human sperm. Chromosoma 102:509–518.
   PubMed Web of Science ®Google Scholar
• Zhang, H., D. N. Roberts, and B. R. Cairns. 2005. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123:219–231.
   PubMed Web of Science ®Google Scholar